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1 Supplementary Information for Encapsulation of a Nerve Agent Detoxifying Enzyme by a Mesoporous Zirconium Metal-Organic Framework Engenders Thermal and Long-Term Stability Peng Li, Su-Young Moon, Mark A. Guelta, Steven P. Harvey, Joseph T. Hupp, Omar K. Farha* *To whom correspondence should be addressed. o-farha@northwestern.edu Table of Contents A Materials and methods S2 B Synthetic procedures S4 C Scanning electron microscopy (SEM) images S6 D Confocal laser scanning microscopy experiments S7 E Catalytic activity experiments S8 F Reference S15 S1
2 A. Materials and methods Materials Zirconyl chloride octahydrate (ZrOCl 2 8H 2 O), N,N-dimethylformamide (DMF), trifluoro acetic acid (TFA), diisopropyl fluorophosphate (DFP), and bis-tris-propane were purchased from Sigma-Aldrich and used as received. AlexaFluor 647 dye was purchased from Life Technologies (Thermo Fisher Scientific). The ligand 4,4',4'',4'''-(ethene-1,1,2,2-tetrayl) tetrakis (([1,1'-biphenyl]-4-carboxylic acid)) (H4ETTC) and PCN-128y were synthesized following the published procedure. 1 The gene encoding the OPAA enzyme was originally cloned from Alteromonas sp. JD6.5, as described previously. 2 Physical methods and measurements Powder X-ray diffraction (PXRD) data were collected on a Rigaku model ATX-G diffractometer equipped with a Cu rotating anode X-ray source. N 2 sorption isotherm measurements were performed on a Micromeritics Tristar II 3020 (Micromeritics, Norcross, GA) at 77 K. Between 30 and 50 mg of material was used for each measurement. 31 P NMR spectrum was recorded on an Agilent 400 FT-NMR spectrometer (400 MHz). Scanning electron microscopy (SEM) images and energy dispersive spectroscopy (EDX) profiles were collected on a Hitachi SU8030. Samples were activated and coated with OsO4 to ~8 nm thickness in a Denton Desk III TSC Sputter Coater (Moorestown, NJ) before SEM-EDX analysis. Inductively coupled plasma atomic emission spectroscopy (ICP-AES) was performed on a computer-controlled (QTEGRA software v. 2.2) Thermo icap 7600 Duo ICP-OES (Thermo Fisher Scientific, S2
3 Waltham, MA, USA) operating in standard mode and equipped with a SPRINT valve and CETAC 520 autosampler (Teladyne CETAC, Omaha, NE, USA). OPAA@PCN-128y samples (2-3 mg ) were digested in a small amount (1 ml) of a mixture of 3:1 v/v conc. HNO 3 :H 2 O 2 (30 wt % in H 2 O) by heating in a Biotage (Uppsala, Sweden) SPX microwave reactor (software version 2.3, build 6250) at 150 C for 5 minutes. The acidic solution was then diluted to a final volume of 15 ml with ultrapure deionized H 2 O and analyzed for S ( , , and nm) and Zr ( , , and nm) content as compared to the standard solutions. The enzymes loading is determined by comparing the experimental Zr:S ratio to the theoretical ratio given by the stoichiometry of Zr in the MOF to the number of methionines and cysteines thiols present in OPAA. S3
4 B. Synthetic procedures OPAA expression. The OPAA gene utilized is a naturally occurring variant. It differs from previous OPAA entry Q by three amino acids at sites 210, 211, and 314. The present gene, which we modified by site-directed mutagenesis, lacks the last 77 carboxyl-terminal amino acids of the OPAA enzyme. This truncated gene was cloned into the NcoI and EcoRI sites of the pse420 expression vector of E. coli. Buffered aqueous solutions of OPAA ( mg/ml) were prepared at ph of 7.2 (tris-bis propane buffer). The sequence of wild type OPAA is shown as below. M N K L A V L Y A E H I A T L Q K R T R E I I E R E N L D G V V F H S G Q A K R 40 Q F L D D M Y Y P F K V N P Q F K A W L P V I D N P H C W I V A N G T D K P K L 80 I F Y R P V D F W H K V P D E P N E Y W A D Y F D I E L L V K P D Q V E K L L P 120 Y D K A R F A Y I G E Y L E V A Q A L G F E L M N P E P V M N F Y H Y H R A Y K 160 T Q Y E L A C M R E A N K I A V Q G H K A A R D A F F Q G K S E F E I Q Q A Y L 200 L A T Q H S E N D T P Y G N I V A L N E N C A I L H Y T H F D R V A P A T H R S 240 F L I D A G A N F N G Y A A D I T R T Y D F T G E G E F A E L V A T M K Q H Q I 280 A L C N Q L A P G K L Y G E L H L D C H Q R V A Q T L S D F N I V N L S A D E I 320 V A K G I T S T F F P H G L G H H I G L Q V H D V G G F M A D E Q G A H Q E P P 360 E G H P F L R C T R K I E A N Q V F T I E P G L Y F I D S L L G D L A A T D N N 400 Q H I N W D K V A E L K P F G G I R I E D N I I V H E D S L E N M T R E L E L D 440 Labeling OPAA with fluorescent dye. AlexaFluor-647 labeled OPAA (OPAA647) was prepared by reacting 0.5 mg OPAA with 1.2 equivalents of an AlexaFluor-647-(ethyl-p-nitrophenyl)-phosphonate conjugate followed by purification of the labeled protein by size-exclusion chromatography (SEC). AlexaFluor-647 was chosen due to the relative insensitivity of its fluorescence intensity and quantum yield to environmental conditions, and excitation / emission maxima (650 nm / 665 nm) that occur far outside that of PCN-128 (400 nm / 540 nm). 1 S4
5 OPAA immobilization in PCN-128y. 1 mg of activated PCN-128y was added to 1 ml of deionized water and sonicated for 5 min until a uniform suspension was formed. The well dispersed solid was isolated by centrifugation at rpm for 1 min and the supernatant was decanted. The solid was then suspended in a 1ml solution of OPAA (0.2 mg/ml) in BTP buffer solution (ph 7.2). The absorbance of the supernatant solution at 280 nm was recorded over 24 h using a NanoDrop 2000 UV-Vis spectrophotometer. After that, the OPAA@PCN-128y composite was isolated by centrifugation at rpm for 1 min, and the supernatant was removed. The solid was further washed with BTP buffer (ph 7.2) 5 times before further experiments. Figure. S1. Concentration of OPAA in solution over time in the presence of 1 mg of PCN-128y exposed to 1ml 0.2mg/ml OPAA solution. S5
6 C. Scanning electron microscopy (SEM) images Figure. S2. SEM images of PCN-128y (top) and (bottom). S6
7 D. Confocal laser scanning microscopy experiemnts Confocal laser scanning microscopy analysis (CLSM) was performed on 10µm-long PCN-128y crystals to examine the distribution of enzymes throughout the matrix. Fluorescence was examined, applying CLSM on a Leica TCS SP5. The Ar laser was set to 5%. Bit depth was set to 12 to achieve 4096 grey levels intensity resolution. Laser line 633 with 3% laser power was used to visualize AlexaFluor-647 dye labeled OPAA on PCN-128y at different depth along z direction. Figure. S3. Confocal laser scanning microscopy images of 20 continuous layers across 3 µm for OPAA647 in PCN-128y. Scale bar depicted is 10 µm. S7
8 E. Catalytic activity experiments Hydrolysis activity for DFP: Hydrolysis profiles of diisopropyl fluorophosphate (DFP) by using free OPAA or immobilized were recorded on an Agilent 400 FT-NMR spectrometer (400 MHz) based on the 31 P NMR spectrum. The 31 P NMR spectrum for DFP consists of a doublet (-7.62 ppm and ppm) due to the phosphorus-fluorine coupling. After the phosphorus-fluorine bond is hydrolyzed by OPAA, the spectrum consists entirely of a downfield singlet from the diisopropylphosphate (-0.95 ppm) (Figure S3). 3 For a typical reaction, composite OPAA@PCN-128y (0.1 mg OPAA and 1 mg PCN-128y) was loaded into a 1.5 dram vial. Then 896 µl of BTP buffer (ph 7.2) and 100µL deuterium water were added, and the reaction mixture was stirred for 1 min to disperse the MOF particles homogeneously, and then 4 µl (22 µmol) of DFP was added and the reaction mixture was swirled for 10 s. The reaction mixture was then transferred to a NMR tube and the spectrum was immediately measured; the first data point was collected 120 s after the start of the reaction. The progress of the reaction was monitored with 1 min increments for 30 min (number of scans = 16, delay time = 28 s). The degree of completion was assessed by calculating the ratio between integration of the product and the reactant peaks based on 31 P NMR. (percent conversion = product peak integral/(substrate + product peak integral) 100). S8
9 Figure S4. A typical time dependent 31 P NMR spectras of hydrolysis of DFP by OPAA or OPAA@PCN-128 S9
10 Different enzyme loading test. Given that 12wt% is the maximum OPAA loading capacity for PCN-128y, we prepared two subsaturated composites by soaking 2 mg PCN-128y in 1 ml buffer solution of 0.1mg/ml OPAA or 0.2 mg/ml OPAA respectively. The complete immobilization of OPAA was monitored until the concentration of OPAA in supernatant becomes zero. The two composites containing 0.1 mg OPAA and 0.2 mg OPAA were then isolated by centrifugation and measured in terms of conversion of DFP hydrolysis as described above. Figure. S5 Hydrolysis of DFP over time by free OPAA (top) and OPAA@PCN-128 (bottom) incubated in BTP buffer (ph 7.2) at different temperatures S10
11 Thermal stability and long-term stability test. For thermal stability, free OPAA or composite containing 0.1mg OPAA was incubated in BTP buffer solution at different temperature, namely 25 o C, 35 o C, 45 o C, 55 o C, and 70 o C for 30 min. For the long-term stability, free OPAA was lyophilized into dry powder sample, and OPAA@PCN-128y was isolated by centrifugation into solid sample. Both of them were left in air at room temperature for different time period, namely 0 day (as-synthesized), 1 day, 3 days, 5 days, and 7 days. The stability of above prepared samples were measured in terms of conversion of DFP hydrolysis as described above. S11
12 Figure. S6 Hydrolysis of DFP over time by free OPAA (top) and (bottom) incubated in BTP buffer (ph 7.2) at different temperatures. S12
13 Figure. S7 Hydrolysis of DFP over time by dried free OPAA (top) and stored at room temperature for different time (days). S13
14 Hydrolysis activity for GD. Kinetic constants for soman (GD) was determined by monitoring the release of free fluoride at 25 C in 50 mm bis-tris-propane buffer, ph 8.0, using a fluoride electrode. Initial screenings were conducted using a single fixed 3.0 mm substrate concentration. 4 Figure. S8 Hydrolysis of soman by OPAA@PCN-128y with different catalyst dose and background reaction. S14
15 F. Reference 1. Zhang, Q.; Su, J.; Feng, D.; Wei, Z.; Zou, X.; Zhou, H.-C., J. Am. Chem. Soc. 2015, 137, (32), Daczkowski, C. M.; Pegan, S. D.; Harvey, S. P., Biochemistry 2015, 54, (41), Dumas, D.P., Wild, J.R. and Raushel, F.M., Biotechnology and applied biochemistry, (2), Tsai, P.C., Fox, N., Bigley, A.N., Harvey, S.P., Barondeau, D.P. and Raushel, F.M., Biochemistry 2012, 51(32), S15
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